Botrytis cinerea, the causative agent of gray mold disease (GMD), invades plants to obtain nutrients and disseminates through airborne conidia in nature. Bacillus amyloliquefaciens strain GD4a, a beneficial bacterium isolated from switchgrass, shows great potential in managing GMD in plants. However, the precise mechanism by which GD4a confers benefits to plants remains elusive. In this study, an A. thaliana-B. cinerea-B. amyloliquefaciens multiple-scale interaction model was used to explore how beneficial bacteria play essential roles in plant growth promotion, plant pathogen suppression, and plant immunity boosting. Arabidopsis Col-0 wild-type plants served as the testing ground to assess GD4a’s efficacy. Additionally, bacterial enzyme activity and targeted metabolite tests were conducted to validate GD4a’s potential for enhancing plant growth and suppressing plant pathogens and diseases. GD4a was subjected to co-incubation with various bacterial, fungal, and oomycete pathogens to evaluate its antagonistic effectiveness in vitro. In vivo pathogen inoculation assays were also carried out to investigate GD4a’s role in regulating host plant immunity. Bacterial extracellular exudate (BEE) was extracted, purified, and subjected to untargeted metabolomics analysis. Benzocaine (BEN) from the untargeted metabolomics analysis was selected for further study of its function and related mechanisms in enhancing plant immunity through plant mutant analysis and qRT-PCR analysis. Finally, a comprehensive model was formulated to summarize the potential benefits of applying GD4a in agricultural systems. Our study demonstrates the efficacy of GD4a, isolated from switchgrass, in enhancing plant growth, suppressing plant pathogens and diseases, and bolstering host plant immunity. Importantly, GD4a produces a functional bacterial extracellular exudate (BEE) that significantly disrupts the pathogenicity of B. cinerea by inhibiting fungal conidium germination and hypha formation. Additionally, our study identifies benzocaine (BEN) as a novel small molecule that triggers basal defense, ISR, and SAR responses in Arabidopsis plants. Bacillus amyloliquefaciens strain GD4a can effectively promote plant growth, suppress plant disease, and boost plant immunity through functional BEE production and diverse gene expression.

Managing soil-borne pathogens and diseases in plants is particularly challenging because the pathogens that cause them can persist in the soil for extended periods, often resulting in repeated crop damage in affected areas. These destructive diseases compromise plant health by weakening the root systems, which makes the plants more susceptible to environmental stress and nutritional deficiencies. Every year in the United States, a whopping $9.6 million is allocated to reverse the harmful effects of pesticides on humans, plants, animals, and the environment. On the contrary, disease-suppressive soils offer an effective strategy for controlling pathogens while ensuring the least contamination of the environment. These soils can be managed by both conventional and advanced methods, such as reduced tillage, crop rotation, organic amendments, nanoparticles, omics approaches, and biofumigation. However, these soils can be local in nature, and their properties might be disrupted by common agricultural practices like tillage and agro-chemical application. This review synthesizes the concepts and mechanisms of disease suppression in soils and explores the ways that can be improved through the management of soil health for enhanced plant health and yield.